Hydrogen peroxide facilitates Arabidopsis seedling establishment by interacting with light signalling pathway in the dark

Light is essential for the plant establishment. Arabidopsis seedlings germinated in the dark cannot grow leaf and only have closed cotyledons. However, exogenous application of H2O2 can induce leaves (establishment) in the dark. Comparative transcriptomic analysis revealed that light-responsive genes were activated by H2O2 treatment. These genes are functionally correlated with photosynthesis, photorespiration, and components of photosystem, such as antenna proteins and light-harvesting chlorophyll proteins. We further found that application of H2O2 facilitates cell cycle by accelerating G(2)-M checkpoint transition in shoot apical meristem. Phytochrome-mediated light signalling pathway was also involved in the H2O2-facilitated establishment process. The constitutive photomorphogenesis 1 and phytochrome interacting factor 3 proteins were shown to be down-regulated by H2O2 treatment and accordingly removed their inhibitory effects on photomorphogenesis in the dark. The crosstalk between oxidation and light signal pathways explains the mechanism that H2O2 regulates plant dark establishment. The endogenous photorespiratory H2O2 production was mimicked by overexpression of glycolate oxidase genes and supplement of substrate glycolate. As expected, seedling establishment was also induced by the endogenously produced H2O2 under dark condition. These findings also suggest that photorespiratory H2O2 production is at least partially involved in postgermination establishment.